Abstract

Individuals within monogamous species form bonds that may buffer against the negative effects of stress on physiology and behavior. In some species, involuntary termination of the mother-offspring bond results in increased symptoms of negative affect in the mother, suggesting that the parent-offspring bond may be equally as important as the pair bond. To our knowledge, the extent to which affect in paternal rodents is altered by involuntary termination of the father-offspring bond is currently unknown. Here, we investigated to what extent separation and paternal experience alters passive stress-coping behaviors and dendritic morphology in hippocampal subfields of California mice (Peromyscus californicus). Irrespective of paternal experience, separated mice displayed shorter latencies to the first bout of immobility, longer durations of immobility, and more bouts of immobility than control (non-separated) mice. This effect of separation was exacerbated by paternal experience in some measures of behavioral despair—separation from offspring further decreased the latency to immobility and increased bouts of immobility. In the dentate gyrus, separation reduced dendritic spine density regardless of paternal experience. Increased spine density was observed on CA1 basal, but not apical, dendrites following paternal experience. Regardless of offspring presence, fatherhood was associated with reduced apical dendritic spine density in area CA3 of the hippocampus. Separation enhanced complexity of both basal and apical dendrites in CA1, while fatherhood reduced dendritic complexity in this region. Our data suggest that forced dissolution of the pair bond induces passive stress-coping behaviors and contributes to region-specific alterations in hippocampal structure in California mouse males.

Highlights

  • The formation of a pair bond is one of the strongest relationships observed between two individuals [1]

  • We examined passive stress-coping strategies, during the forced swim test, followed by Golgi-Cox analysis of dendritic morphology in hippocampal subfields (DG, CA1, and CA3) of California mouse males that were separated from their offspring on postnatal day (PND) 1, compared to males that remained with their offspring until weaning

  • We demonstrated that 4–5 weeks of separation reduced dendritic spine density in the dentate gyrus (DG) of male California mice, regardless of paternal experience

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Summary

Introduction

The formation of a pair bond is one of the strongest relationships observed between two individuals [1]. As seen in monogamous species, bonds are typically formed after individuals spend significant periods of time in physical contact with one another [2,3]. These bonds can serve as a social buffer [1], one that may protect from the deleterious effects of stress on physiology and behavior [4]. While bond formation and bond separation studies typically focus on interactions between adults [9], for many species, the parent-offspring bond is an important interaction—one that can have significant and long-lasting effects on offspring development [10] and the structure and function of the parental brain [11,12,13,14]. While some male rodents display parenting behaviors [15, 16], which can result in parenting-induced alterations in brain plasticity [17], it is not known whether benefits of father-offspring interaction are long-lasting or the extent to which preventing this interaction negatively affects neural structure and/or affective behaviors in the paternal brain

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